Evidence for glycolysis in bovine retinal microsome and photoreceptor outer segments

Connell, David G. Mc; Ozga, George W.; Solze, Dale A.

doi:10.1016/0304-4165(69)90093-2

Cited by 16 publications

(4 citation statements)

References 29 publications

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“…In fact the OS is glycolytically active in several species (e.g. McConnell et al, 1969;Hsu & Molday, 1994;Winkler, 1995). The finding that z 1 ϭ 0 implies either that glycolysis in this layer is small compared to other layers, or that protons derived from hydrolysis of anaerobically produced ATP are not extruded by the OS into the extracellular space, but are shuttled to another part of the cell for extrusion or neutralization.…”

Section: Implication Of Modeling Resultsmentioning

confidence: 99%

Quantification of in vivo anaerobic metabolism in the normal cat retina through intraretinal pH measurements

Padnick‐Silver

Linsenmeier

2002

Vis Neurosci

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We examined intraretinal [H+] in the intact retina of anesthetized cats using H+-sensitive microelectrodes to obtain spatial profiles of extracellular [H+]. One H+ is produced when an anaerobically generated ATP is utilized. We theorized that H+ production directly reflects anaerobic glucose consumption. From the choroid (pH approximately 7.40), [H+]o steadily increased to a maximum concentration in the proximal portion of the outer nuclear layer (pH approximately 7.20). The shape of the profile was always concave down, indicating that a net production of H+ occurred across the avascular outer retina. A three-layer diffusion model of the outer retina was developed and fitted to the data to quantify photoreceptor H+ extrusion into the extracellular space (Q(OR-H+)). It was determined that the outer segment (OS) layer had negligible H+ extrusion. The data were then refitted to a special three-layer model in which the OS layer Q(H+) was set equal to zero, but in which the inner segments and outer nuclear layer produced H+. The resulting Q(OR-H+) was several orders of magnitude lower than previous measurements of Q(OR-lactate), which were based on choroidal mass balances of lactate. Stoichiometrically, one H+ is produced for each lactate produced, so we concluded that Q(OR-H+) is a measure of net rather than total H+ production. Because retinal acid production is so high, the retina must contain efficient H+ clearance and/or neutralization mechanisms that prevent severe acidosis. The effect of light on retinal extracellular [H+] and Q(OR-H+) was also examined. As expected, light adaptation caused a retinal alkalinization that resulted from a 52% reduction in Q(OR-H+). This is in agreement with previous studies that have shown that both oxidative (e.g. Haugh et al., 1990) and glycolytic metabolism (Wang et al., 1997a,c) in the photoreceptor are decreased by a factor of 2 during light adaptation. Although we could not obtain absolute values for outer retinal glycolysis, changes in Q(OR-H+) appear to directly reflect changes in glycolytic metabolism.

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Section: Implication Of Modeling Resultsmentioning

confidence: 99%

Quantification of in vivo anaerobic metabolism in the normal cat retina through intraretinal pH measurements

Padnick‐Silver

Linsenmeier

2002

Vis Neurosci

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“…A number of biochemical mechanisms have been identified by which the NADPH economy of rod photoreceptors may be regulated. One synthetic mechanism for the production of NADPH is by glycolysis and the hexose monophosphate pathways that operate within the outer segment (Futterman, 1963;McConnell et al, 1969;Futterman et al, 1970;Schnetkamp and Daemen, 1981;Molday, 1991, 1994). A second mechanism is the phosphocreatine shuttle pathway, which is thought to transport high-energy phosphate groups in the form of creatine phosphate from the inner segment to the outer segment (Hsu and Molday, 1994).…”

Section: Mechanisms Of Reduction Of Retinal To Retinol: Sources Of Nadphmentioning

confidence: 99%

Physiological and Microfluorometric Studies of Reduction and Clearance of Retinal in Bleached Rod Photoreceptors

Tsina

Chen

Koutalos

et al. 2004

The Journal of General Physiology

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The visual cycle comprises a sequence of reactions that regenerate the visual pigment in photoreceptors during dark adaptation, starting with the reduction of all-trans retinal to all-trans retinol and its clearance from photoreceptors. We have followed the reduction of retinal and clearance of retinol within bleached outer segments of red rods isolated from salamander retina by measuring its intrinsic fluorescence. Following exposure to a bright light (bleach), increasing fluorescence intensity was observed to propagate along the outer segments in a direction from the proximal region adjacent to the inner segment toward the distal tip. Peak retinol fluorescence was achieved after ∼30 min, after which it declined very slowly. Clearance of retinol fluorescence is considerably accelerated by the presence of the exogenous lipophilic substances IRBP (interphotoreceptor retinoid binding protein) and serum albumin. We have used simultaneous fluorometric and electrophysiological measurements to compare the rate of reduction of all-trans retinal to all-trans retinol to the rate of recovery of flash response amplitude in these cells in the presence and absence of IRBP. We find that flash response recovery in rods is modestly accelerated in the presence of extracellular IRBP. These results suggest such substances may participate in the clearance of retinoids from rod photoreceptors, and that this clearance, at least in rods, may facilitate dark adaptation by accelerating the clearance of photoproducts of bleaching.

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“…Because the outer segment is devoid of mitochondria, it has been proposed that the energy used in this compartment is supplied by the inner segment by diffusion of ATP through the connecting cilium (Linton et al, 2010). However, the presence of glycolytic enzymes in the outer segment, as determined by biochemical (Hsu and Molday, 1991;Hsu and Molday, 1994;Lowry et al, 1961;McConnell et al, 1969) and immunohistochemical (Hsu and Molday, 1991) methods, suggests that the outer segment is not entirely dependent on inner segment metabolism. Rather, it appears to possess the energy-generating capacity to meet at least some of its own needs through glycolysis.…”

Section: Introductionmentioning

confidence: 99%

Facilitative glucose transporter Glut1 is actively excluded from rod outer segments

Gospe

Baker

Arshavsky

2010

Journal of Cell Science

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SummaryPhotoreceptors are among the most metabolically active cells in the body, relying on both oxidative phosphorylation and glycolysis to satisfy their high energy needs. Local glycolysis is thought to be particularly crucial in supporting the function of the photoreceptor's light-sensitive outer segment compartment, which is devoid of mitochondria. Accordingly, it has been commonly accepted that the facilitative glucose transporter Glut1 responsible for glucose entry into photoreceptors is localized in part to the outer segment plasma membrane. However, we now demonstrate that Glut1 is entirely absent from the rod outer segment and is actively excluded from this compartment by targeting information present in its cytosolic C-terminal tail. Our data indicate that glucose metabolized in the outer segment must first enter through other parts of the photoreceptor cell. Consequently, the entire energy supply of the outer segment is dependent on diffusion of energy-rich substrates through the thin connecting cilium that links this compartment to the rest of the cell.

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Evidence for glycolysis in bovine retinal microsome and photoreceptor outer segments

Cited by 16 publications

References 29 publications

Quantification of in vivo anaerobic metabolism in the normal cat retina through intraretinal pH measurements

Quantification of in vivo anaerobic metabolism in the normal cat retina through intraretinal pH measurements

Physiological and Microfluorometric Studies of Reduction and Clearance of Retinal in Bleached Rod Photoreceptors

Facilitative glucose transporter Glut1 is actively excluded from rod outer segments

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